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Sexual Conflict and Gene Expression in Drosophila melanogaster
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
2011 (English)Doctoral thesis, comprehensive summary (Other academic) [Artistic work]
Abstract [en]

Sexual conflict is broadly defined as a conflict between the evolutionary interests of the two sexes. Depending on the genetic architecture of the traits involved, it can occur at the level of male-female interactions or take the form of selection acting to change the mean of a shared trait against the sign of its genetic correlation. The aim of my thesis was to use genome-wide expression profiles in the model organism Drosophila melanogaster to provide novel insights in the study of sexual conflict.

First, we studied the female post-mating response to partition transcriptional changes associated with reproduction from male-induced effects, which are known to be harmful to females. We found substantial changes in expression of metabolic pathways associated with the activation of reproduction, while male-specific effects were dominated by the onset of an immune response. Changes in female response under different mating strategies was studied using experimental evolution: we found that monogamous females suffered decreased fecundity and their gene expression profiles suggested an overall weaker response to mating. To identify sexually antagonistic genes, we used hemiclonal lines and associated their sex-specific fitness with genome-wide transcript abundance. We confirmed the presence of a negative covariance for fitness and identified a group of candidate genes experiencing sexually antagonistic selection. We then focused on mitochondria, which can enable the accumulation of deleterious mutations with sex-specific effects due to their maternal inheritance, and found few effects on nuclear gene expression in females but major effects in males, predominantly in male-specific tissues. Finally, we used published data to compare intraspecific and interspecific genetic variation for a set of transcripts, to test whether speciation occurs along lines of maximum genetic variance.

In conclusion, gene expression techniques can generate useful results in the study of sexual conflict, particularly in association with phenotypic data or when integrated with published datasets.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis , 2011. , 46 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 843
Keyword [en]
Sexual conflict, sexual selection, male-female coevolution, gene expression, transcriptome, microarrays, sexual dimorphism, Drosophila
National Category
Biological Sciences
Research subject
Biology with specialization in Animal Ecology; Biology with specialization in Evolutionary Genetics
Identifiers
URN: urn:nbn:se:uu:diva-156567ISBN: 978-91-554-8130-8 (print)OAI: oai:DiVA.org:uu-156567DiVA: diva2:432764
Public defence
2011-10-01, Zootissalen, EBC, Villavägen 9, Uppsala, 09:30 (English)
Opponent
Supervisors
Available from: 2011-09-08 Created: 2011-08-03 Last updated: 2011-11-03
List of papers
1. Immunogenic males: a genome-wide analysis of reproduction and the cost of mating in Drosophila melanogaster females
Open this publication in new window or tab >>Immunogenic males: a genome-wide analysis of reproduction and the cost of mating in Drosophila melanogaster females
2009 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 22, no 5, 964-973 p.Article in journal (Refereed) Published
Abstract [en]

In Drosophila melanogaster, mating radically transforms female physiology and behaviour. Post-mating responses include an increase in the oviposition rate, a reduction in female receptivity and an activation of the immune system. The fitness consequences of mating are similarly dramatic - females must mate once in order to produce fertile eggs, but additional matings have a clear negative effect. Previously, microarrays have been used to examine gene expression of females differing in their reproductive status with the aim of identifying genes influenced by mating. However, as only virgin and single mated females were compared, transcriptional changes associated with reproduction (under natural selection) and male-induced effects (possibly under sexually antagonistic selection) cannot be disentangled. We partitioned these fundamentally different effects by instead examining the expression profiles of virgin, single mated and double mated females. We found substantial effects relating to reproduction and further effects that are only attributable to mating itself. Immune response genes dominate this male-induced effect indicating that the cost of mating may be due partly to this system's activation. We propose that both sexually antagonistic and natural selection have been important in the evolution of the innate immunity genes, thereby contributing to the sexual dimorphism and rapid evolution at these loci.

Keyword
BIOCONDUCTOR, cost of mating, Drosophila melanogaster, innate immunity, microarrays, post-mating female response, sexual conflict, sperm competition
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-129120 (URN)10.1111/j.1420-9101.2009.01708.x (DOI)000265252100005 ()
Available from: 2010-08-09 Created: 2010-08-05 Last updated: 2017-12-12Bibliographically approved
2. Genome-wide targets of selection: female response to experimental removal of sexual selection in D. melanogaster
Open this publication in new window or tab >>Genome-wide targets of selection: female response to experimental removal of sexual selection in D. melanogaster
(English)Manuscript (preprint) (Other academic)
Identifiers
urn:nbn:se:uu:diva-156650 (URN)
Available from: 2011-08-05 Created: 2011-08-05 Last updated: 2011-09-08
3. The Sexually Antagonistic Genes of Drosophila melanogaster
Open this publication in new window or tab >>The Sexually Antagonistic Genes of Drosophila melanogaster
2010 (English)In: PLoS biology, ISSN 1544-9173, E-ISSN 1545-7885, Vol. 8, no 3, e1000335- p.Article in journal (Refereed) Published
Abstract [en]

When selective pressures differ between males and females, the genes experiencing these conflicting evolutionary forces are said to be sexually antagonistic. Although the phenotypic effect of these genes has been documented in both wild and laboratory populations, their identity, number, and location remains unknown. Here, by combining data on sex-specific fitness and genome-wide transcript abundance in a quantitative genetic framework, we identified a group of candidate genes experiencing sexually antagonistic selection in the adult, which correspond to 8% of Drosophila melanogaster genes. As predicted, the X chromosome is enriched for these genes, but surprisingly they represent only a small proportion of the total number of sex-biased transcripts, indicating that the latter is a poor predictor of sexual antagonism. Furthermore, the majority of genes whose expression profiles showed a significant relationship with either male or female adult fitness are also sexually antagonistic. These results provide a first insight into the genetic basis of intralocus sexual conflict and indicate that genetic variation for fitness is dominated and maintained by sexual antagonism, potentially neutralizing any indirect genetic benefits of sexual selection.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-136200 (URN)10.1371/journal.pbio.1000335 (DOI)000278125400013 ()
Available from: 2010-12-10 Created: 2010-12-10 Last updated: 2017-12-11Bibliographically approved
4. Experimental Evidence Supports a Sex-Specific Selective Sieve in Mitochondrial Genome Evolution
Open this publication in new window or tab >>Experimental Evidence Supports a Sex-Specific Selective Sieve in Mitochondrial Genome Evolution
2011 (English)In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 332, no 6031, 845-848 p.Article in journal (Refereed) Published
Abstract [en]

Mitochondria are maternally transmitted; hence, their genome can only make a direct and adaptive response to selection through females, whereas males represent an evolutionary dead end. In theory, this creates a sex-specific selective sieve, enabling deleterious mutations to accumulate in mitochondrial genomes if they exert male-specific effects. We tested this hypothesis, expressing five mitochondrial variants alongside a standard nuclear genome in Drosophila melanogaster, and found striking sexual asymmetry in patterns of nuclear gene expression. Mitochondrial polymorphism had few effects on nuclear gene expression in females but major effects in males, modifying nearly 10% of transcripts. These were mostly male-biased in expression, with enrichment hotspots in the testes and accessory glands. Our results suggest an evolutionary mechanism that results in mitochondrial genomes harboring male-specific mutation loads.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-154276 (URN)10.1126/science.1201157 (DOI)000290529900047 ()21566193 (PubMedID)
Available from: 2011-05-30 Created: 2011-05-30 Last updated: 2017-12-11Bibliographically approved
5. Interspecific divergence of gene networks along lines of genetic variance in Drosophila: dimensionality, evolvability and constraints.
Open this publication in new window or tab >>Interspecific divergence of gene networks along lines of genetic variance in Drosophila: dimensionality, evolvability and constraints.
(English)Manuscript (preprint) (Other academic)
Identifiers
urn:nbn:se:uu:diva-156651 (URN)
Available from: 2011-08-05 Created: 2011-08-05 Last updated: 2011-09-08

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